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The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase

Author

Listed:
  • Takafumi Kawai

    (Osaka University)

  • Shin Morioka

    (Tokyo Medical and Dental University)

  • Haruhiko Miyata

    (Osaka University)

  • Rizki Tsari Andriani

    (Osaka University)

  • Sharmin Akter

    (Osaka University
    Bangladesh Agricultural University)

  • Gabriel Toma

    (Osaka University
    Osaka University)

  • Tatsuya Nakagawa

    (Osaka University
    Osaka University)

  • Yuki Oyama

    (Osaka University
    Osaka University)

  • Rie Iida-Norita

    (Osaka University)

  • Junko Sasaki

    (Tokyo Medical and Dental University)

  • Masahiko Watanabe

    (Hokkaido University)

  • Kenji Sakimura

    (Niigata University)

  • Masahito Ikawa

    (Osaka University
    Osaka University)

  • Takehiko Sasaki

    (Tokyo Medical and Dental University)

  • Yasushi Okamura

    (Osaka University
    Osaka University)

Abstract

Voltage-sensing phosphatase (VSP) exhibits voltage-dependent phosphatase activity toward phosphoinositides. VSP generates a specialized phosphoinositide environment in mammalian sperm flagellum. However, the voltage-sensing mechanism of VSP in spermatozoa is not yet characterized. Here, we found that VSP is activated during sperm maturation, indicating that electric signals in immature spermatozoa are essential. Using a heterologous expression system, we show the voltage-sensing property of mouse VSP (mVSP). The voltage-sensing threshold of mVSP is approximately −30 mV, which is sensitive enough to activate mVSP in immature spermatozoa. We also report several knock-in mice in which we manipulate the voltage-sensitivity or electrochemical coupling of mVSP. Notably, the V312R mutant, with a minor voltage-sensitivity change, exhibits abnormal sperm motility after, but not before, capacitation. Additionally, the V312R mutant shows a significant change in the acyl-chain profile of phosphoinositide. Our findings suggest that electrical signals during sperm maturation are crucial for establishing the optimal phosphoinositide environment in spermatozoa.

Suggested Citation

  • Takafumi Kawai & Shin Morioka & Haruhiko Miyata & Rizki Tsari Andriani & Sharmin Akter & Gabriel Toma & Tatsuya Nakagawa & Yuki Oyama & Rie Iida-Norita & Junko Sasaki & Masahiko Watanabe & Kenji Sakim, 2024. "The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51755-2
    DOI: 10.1038/s41467-024-51755-2
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    References listed on IDEAS

    as
    1. Yuriy Kirichok & Betsy Navarro & David E. Clapham, 2006. "Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel," Nature, Nature, vol. 439(7077), pages 737-740, February.
    2. Yoshimichi Murata & Hirohide Iwasaki & Mari Sasaki & Kazuo Inaba & Yasushi Okamura, 2005. "Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor," Nature, Nature, vol. 435(7046), pages 1239-1243, June.
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